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Right-To-Left Shunt Has Modest Effects on C02 Delivery to the Gut Coversheet This is the publisher’s PDF (Version of Record) of the article. This is the final published version of the article. How to cite this publication: Christian Lind Malte, Hans Malte, Lærke Rønlev Reinholdt, Anders Findsen, James W. Hicks, Tobias Wang (2017). ”Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery.” Journal of Experimental Biology, 220, 531-536. https://doi.org/10.1242/jeb.149625 Publication metadata Title: Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery. Author(s): Christian Lind Malte, Hans Malte, Lærke Rønlev Reinholdt, Anders Findsen, James W. Hicks, Tobias Wang Journal: Journal of Experimental Biology DOI/Link: https://doi.org/10.1242/jeb.149625 Document version: Publisher’s PDF (Version of Record) This article has been published in Journal of Experimental Biology. © 2017 Published by The Company of Biologists Ltd Redistribution subject to Journal of Experimental Biology license or copyright; see Terms of Use at http://jeb.biologists.org/content/rights-permissions General Rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognize and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. If the document is published under a Creative Commons license, this applies instead of the general rights. This coversheet template is made available by AU Library Version 1.0, December 2017 © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 531-536 doi:10.1242/jeb.149625 SHORT COMMUNICATION Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery Christian Lind Malte1,*, Hans Malte1, Lærke Rønlev Reinholdt1, Anders Findsen1, James W. Hicks2 and Tobias Wang1 ABSTRACT digestion may be an exception. A combination of unique anatomical By virtue of their cardiovascular anatomy, reptiles and amphibians features of the crocodilian cardiovascular system (Hicks, 1998) can shunt blood away from the pulmonary or systemic circuits, but the combined with physiological measurements fostered the idea that – functional role of this characteristic trait remains unclear. It has been increased R L shunts serve to fuel the gastric mucosa with acidic suggested that right-to-left (R–L) shunt (recirculation of systemic proton-rich blood during digestion in alligators (Farmer et al., 2008; blood within the body) fuels the gastric mucosa with acidified and Gardner et al., 2011; Jones and Shelton, 1993). Central to this proposal is the observation that the crocodilian coeliac artery CO2-rich blood to facilitate gastric acid secretion during digestion. – appears as a continuation of the left aortic arch, which indicates that However, in addition to elevating PCO2,RL shunt also reduces the stomach is preferentially perfused with CO2-rich blood from the arterial O2 levels and would compromise O2 delivery during the increased metabolic state of digestion. Conversely, arterial P can right ventricle (e.g. Jones, 1996; Webb, 1979). In support for CO2 P also be elevated by lowering ventilation relative to metabolism (i.e. elevated (systemic) arterial partial pressure of CO2 ( CO2) reducing the air convection requirement, ACR). Based on a governing acid secretion, Farmer et al. (2008) reported slower mathematical analysis of the relative roles of ACR and R–L shunt digestion after surgical removal of the left aorta in alligators. However, a number of other studies show that growth is not affected on O2 and CO2 levels, we predict that ventilatory modifications are by similar procedures (Eme et al., 2009, 2010), and it is possible much more effective for gastric CO2 supply with only modest effects that the slower digestion stems from reduced perfusion of the on O2 delivery. Conversely, elevating CO2 levels by means of R–L gastrointestinal organs after occlusion of the left aortic arch (Hicks shunt would come at a cost of significant reductions in O2 levels. The and Wang, 2012). different effects of altering ACR and R–L shunt on O2 and CO2 levels are explained by the differences in the effective blood capacitance Although the cardiovascular system must simultaneously provide – coefficients. for O2 delivery and CO2 removal, the proposition that R L shunts assist gastric acid secretion has not included considerations of the KEY WORDS: Gas exchange, Heart, Mathematical model, Reptile, inexorable reduction in O2 delivery. R–L shunts cause large Shunting reduction in arterial O2 levels – whether expressed as partial pressure, O2 concentration or haemoglobin saturation (Wang and INTRODUCTION – P Hicks, 1996) while the effects on arterial CO2 are predicted to be The ability to shunt blood away from the pulmonary or systemic considerably smaller given the high capacitance coefficient for CO2 circulations is a defining character of the reptilian and amphibian in blood. An increased R–L shunt during digestion would therefore cardiovascular systems (Hicks, 1998). However, whilst much is also compromise O2 delivery, which seems undesirable given the known about the anatomical basis for central vascular shunts and fourfold elevation in O2 demands during digestion (Busk et al., their autonomic regulation, the functional role of bypassing one or 2000). In this context, it may be more prudent to elevate arterial P the other circulation remains as mysterious as it is debated (Hicks CO2 by means of ventilation [i.e. a lowering of the air convection and Wang, 2012). Thus, it remains uncertain as to whether this requirement (ACR) for CO2], a response that has been suggested to cardiovascular design is an exquisite adaptation to low ectothermic compensate for the rise in plasma bicarbonate during digestion (the metabolism and intermittent pulmonary ventilation, or merely an so-called ‘alkaline tide’; Hicks et al., 2000; Hicks and White, 1992; atavistic relict with no particular functional benefits (Hicks and Wang et al., 2001b). However, decreasing the ACR to elevate CO2 P Wang, 2012). levels will simultaneously lower the lung O2 and could negatively In several species of reptiles and amphibians, the right-to-left (R– impact O2 delivery. L) shunts (i.e. the direct recirculation of systemic venous blood into To address the compromise between adequate O2 delivery and the arterial systemic circulation) decrease whenever oxygen arterial acid–base status, we developed an integrated numerical demands are elevated (Hicks and Wang, 2012). However, in model that can be applied to amphibians and reptiles, to provide a crocodilians, an elevated oxygen consumption associated with quantitative comparison of the effects of R–L shunting and altered ventilation on blood O2 and CO2 levels. 1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, MATERIALS AND METHODS Denmark. 2Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA. Fig. 1A illustrates the model of gas exchange for O2 and CO2 based on mass balances and relationships that express electro-neutrality in *Author for correspondence ([email protected]) blood compartments. The model does not include diffusion C.L.M., 0000-0002-7003-6370 limitations or spatial heterogeneities at tissues or lungs, and incorporates a thermodynamically correct description of the Received 12 September 2016; Accepted 6 December 2016 Bohr–Haldane effect. Journal of Experimental Biology 531 SHORT COMMUNICATION Journal of Experimental Biology (2017) 220, 531-536 doi:10.1242/jeb.149625 C The total concentration of CO2 in blood ( bCO2) is the sum of the List of symbols and abbreviations α P physically dissolved CO2 ( CO2 CO2) and the bicarbonate and ACR air convection requirement carbonate concentration, as quantified by the equilibrium constants C , concentration of CO or O in the pulmonary artery K K + PaCO2 2 2 of CO2 hydration ( 1 and 2) and the proton concentration ([H ], CPaO2 S which is related to O2): CPvCO2, concentration of CO2 or O2 in pulmonary venous return (i.e. ! C left atrium) PvO2 K1 K1K2 C , concentration of CO or O in the systemic arterial blood C ¼ a P 1 þ þ : ð10Þ SaCO2 2 2 bCO2 CO2 CO2 ½Hþ ½ þ2 CSaO2 H CSvCO2, concentration of CO2 or O2 in systemic venous return (i.e. C right atrium) SvO2 Electro-neutrality in blood Hb haemoglobin Lshunt gas exchange limitation imposed by shunts Equations that express electro-neutrality were derived by p number of Bohr-groups of haemoglobin conservation of charge, where electro-neutrality in a given blood i PACO2, partial pressure of CO2 or O2 in the lung gas compartment (subscript ) is given below: ! PAO2 P , P partial pressure of CO or O in a given compartment K K K K CO2 O2 2 2 ½ þ þ ¼ w þ a P 1 þ 2 1 2 P , P inspired partial pressure of CO or O H i SID þ CO2 CO2i þ ICO2 IO2 2 2 ½ ½ þ 2 _ H i H i ½H i QLR left-to-right shunt flow _ þ Qpul pulmonary blood flow þ b ð Þ ÞpC S ; ð Þ _ NB log(1/[H i pHiso Hb Hi 11 QRL right-to-left shunt flow _ Qsys systemic blood flow where SID is the strong-ion difference (Stewart, 1978), Kw is the Q_ total cardiac output tot ionic product of water, βNB is the non-bicarbonate buffer capacity, R–L right-to-left shunt pHiso is the pH of zero net charge of the buffer groups, SH is the Rperf blood convective/perfusive resistance p RQ respiratory quotient fractional saturation of haemoglobin with protons and is the number of Bohr-groups of haemoglobin.
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